A remarkable legion of guests: Diversity and host specificity of army ant symbionts (Author Summary)

A myrmecoid, or ant mimicking, staphylinid beetle, Ecitophya simulans, grooms an Eciton burchellii army ant worker. This beetle occurs with a single army ant host species, Eciton burchellii. Photo credit: Daniel Kronauer

Tropical rainforests are teeming with life, and species inventories are far from complete. We know even less about the intricate ecological interactions that form the basis of tropical communities. One fascinating but poorly studied example is the host-symbiont network between army ants and their rich assemblages of arthropod guests. In issue 20 of Molecular Ecology, we studied the biodiversity and host specificity of such a network in a Costa Rican rainforest. Combining DNA barcoding with morphological identification, we discovered 62 species parasitizing the six available Eciton army ant host species, including beetles, flies, a millipede, and a silverfish. At least 14 of these species were new to science. Host specificity varied markedly, ranging from specialists parasitizing a single host, to host generalists occurring with all available host species. This highlights the immense diversity of army ant guests, both in terms of their species numbers and their ecological interactions with the ants. Like many of their cohabitants in tropical ecosystems, army ants are sensitive to habitat degradation, and extinction of the ants will go hand in hand with an extinction cascade of their numerous guests. We must therefore enhance our efforts to protect tropical rainforests to preserve such marvelous host-symbiont systems.

Article: Christoph von Beeren, Nico Blüthgen, Philipp O. Hoenle, Sebastian Pohl, Adrian Brückner, Alexey K. Tishechkin, Munetoshi Maruyama, Brian V. Brown, John M. Hash, W. E. Hall, Daniel J. C. Kronauer (2021). A remarkable legion of guests: Diversity and host specificity of army ant symbionts. Molecular Ecology30(20), 5229-5246. https://doi.org/10.1111/mec.16101

Summary written by Christoph von Beeren

A symbiotic staphylinid beetle, Proxenobius borgmeieri, runs among army ant workers in an emigration column of its single host species, Eciton hamatum. Photo credit: Daniel Kronauer
A symbiotic featherwing beetle, Cephaloplectus mus, sits on the head of an army ant queen (Eciton burchellii). This host generalist parasitizes all six Eciton army ant species in Costa Rica. Photo credit: Daniel Kronauer

Summary from the authors: Estimating contemporary effective population size

Effective population size (Ne) is crucial parameter in evolutionary biology that reflects the number of individuals in a theoretically ideal population having the same magnitude of loss of genetic variation as the population in question. There are several types of Ne estimates, and they vary in definition and application. For example, contemporary Ne represents the size of a population in the previous generation/s and is a parameter of relevance in many species. Estimating contemporary Ne is, however, difficult and remains in practice often unknown. This is particularly the case for large populations where the amount of drift in the short term is limited. We used genomic data from 85 collared flycatchers of an island population sampled at two time points, and applied several methods to estimate Ne. These methods either compared genetic variation between the two time points (temporal methods) or analyzed variation patterns from a single time point (LD-based methods). The temporal methods estimated Ne at a level of few thousand, while the approach based on LD provided ambiguous estimates associated with high variance. Our results suggest that whole-genome data can help to estimate large contemporary Ne, but temporal sampling seems to be necessary.  

Article: Nadachowska-Brzyska K, Dutoit L, Smeds L, Kardos M, Gustafsson L, Ellegren H. 2021. Genomic inference of contemporary effective population size in a large island population of collared flycatchers (Ficedula albicollis). Molecular Ecology https://doi.org/10.1111/mec.16025.

Summary from the authors: landscape genetics of eastern indigo snakes

Landscape features, such as land use, vegetation cover, roads, and topography, strongly influence genetic connectivity yet these relationships can vary across spatial scales which therefore requires multi-scale approaches for evaluating landscape genetics relationships. We used the federally threatened eastern indigo snake (Drymarchon couperi), a terrestrial habitat generalist endemic to the southeastern United States, as a case study with which to evaluate the consequences of different approaches for accounting for spatial scale when optimizing genetics resistance surfaces using the software ResistanceGA. Resistance surfaces with scale selected using a true optimization approach simultaneously comparing all possible combinations of scale across each set of covariates performed better than resistance surfaces where scale was selected individually for each covariate. Truly optimized resistance surfaces also outperformed resistance surfaces based on habitat selection models and categorical land cover maps. Optimal scales were usually larger than average indigo snake home range sizes suggesting that gene flow was mediated mostly by extra-home range dispersal. Large tracts of undeveloped upland habitat with intermediate habitat heterogeneity most promoted indigo snake gene flow while roads did not appear to restrict gene flow. Our results show the importance of testing a wide range of spatial scales in landscape genetics studies. 

The top-ranked optimized genetic resistance surfaces for eastern indigo snakes in central Florida from (a) categorical land cover surfaces, (b) multi-scale habitat selection models, and (c) multi-scale landscape covariates selected using a true optimization approach. (d) shows an average resistance surface across our best-supported truly optimized resistance surfaces. (Figure 6 from Bauder et al. 2021.)

Article: Bauder JM, Peterman WE, Spear SF, Jenkins CL, Whiteley AR, McGarigal K. 2021. Multiscale assessment of functional connectivity: Landscape genetics of eastern indigo snakes in an anthropogenically fragmented landscape in central Florida. Molecular Ecology https://doi.org/10.1111/mec.15979.

Summary from the authors: Detecting selected haplotype blocks in evolve and resequence experiments

How organisms adapt to changes in the environment is not only a central question of evolutionary biology but also relevant to the threat of recent global warming. Evolution experiments in controlled laboratory settings (Experimental Evolution) are a great tool for evaluating evolutionary processes. When combined with genome sequencing (Evolve and Resequence), genomic changes related to adaptation can be identified. Although these genomic changes can occur in large parts of a chromosome (selected haplotype block), most approaches focus only on single genomic sites, and in consequence might overestimate the signal of evolution. Here, we present a novel method for detecting such selected haplotype blocks in evolve and resequence experiments. Our approach requires only few input parameters and is based on the grouping of neighboring genomic sites and on a comparison of different chromosomes. Analyzing computer simulations and experimental data, we describe distinct haplotype block patterns related to the number of genomic sites under selection and to the speed of adaptation. Our results indicate that the analysis of selected haplotype blocks has indeed the potential to deepen our understanding of adaptation.

Read the full text here.

Figure 1: Left: Flies are a powerful model organism to study temperature adaptation from standing genetic variation in evolve and resequence experiments (modified from Mallard et al., 2018). Right: Selected haplotype blocks (blue) spanning large parts of a chromosome are present in the majority of individuals after 60 generations of experimental evolution.

References

Otte KA, Schlötterer C. Detecting selected haplotype blocks in evolve and resequence experiments. Mol Ecol Resour. 2021;21:93–109. https://doi.org/10.1111/1755-0998.13244

Mallard, François, et al. A simple genetic basis of adaptation to a novel thermal environment results in complex metabolic rewiring in Drosophila. Genome biology 2018:19.1: 1-15. https://doi.org/10.1186/s13059-018-1503-4.

Summary from the authors: A linked-read approach to museomics: Higher quality de novo genome assemblies from degraded tissues

We aimed to sequence and compare all the DNA (eg., the genome) of a bunch of different deer mice (genus Peromyscus) species to understand how some deer mice survive in hot deserts with little to no water. A number of deer mice tissue samples were available through natural history museums, which house the raw materials for genetic and biodiversity investigations, but the samples had been collected many years earlier. Older samples produce lower quality DNA that has been broken into many pieces over time. Our normal sequencing procedure selectively removes small fragments of DNA, which would essentially throw away all the DNA we wanted to sequence for these older samples! To circumvent this, we were able to use a different DNA library preparation method called linked-read sequencing (LRS). LRS uses standard short-read sequencing technology, but adds additional information about the location of DNA fragments within the genome by bundling and barcoding DNA fragments that are located near each other prior to sequencing (eg., ‘links’ DNA fragments together in ‘genome-space’). We found that this method improves the overall quality and completeness of genome assemblies from historical tissue samples, in less time and with less effort than traditional shot-gun sequencing methods. This alternative method may be particularly valuable for building high-quality genome assemblies for extinct species for which there are no new samples being collected for or endangered species that are difficult to sample or collect. LRS adds to the suite of genomic methods that continue to unlock the secrets of natural history collections and enable fine-scale genetic measurement of change through time.

This summary was written by the study’s first author, Jocelyn Colella.

Read the full text here.

Video credit: Jocelyn Colella. Peromyscus in the field.

Full Text: Colella JP, Tigano A, MacManes MD. A linked-read approach to museomics: Higher quality de novo genome assemblies from degraded tissues. Mol Ecol Resour. 2020;20:871–881.

Summary from the authors: A metagenomic assessment of microbial eukaryotic diversity in the global ocean

Marine microbial eukaryotes are key components of planktonic ecosystems in all ocean biomes. They are, along with cyanobacteria, responsible for nearly half of the global primary production, and play important roles in food-web dynamics as grazers and parasites, carbon export to the deep ocean, and nutrient remineralization. Currently, one of the most common approaches to survey their diversity is sequencing marker genes amplified from genomic DNA extracted from microbial assemblages. However, this approach requires a PCR step, which is known to introduce biases in microbial diversity estimates. One alternative to overcome this issue involves exploiting the taxonomic information contained in metagenomes, which use massive shotgun sequencing of the same DNA extracts with the goal of assessing the putative functions of environmental microbes.

In this study we investigated the potential of metagenomics to provide taxonomic reports of marine microbial eukaryotes. The overall diversity reported by this approach was similar to that obtained by amplicon sequencing, although the latter performed poorly for some taxonomic groups. We then studied the diversity of picoeukaryotes and nanoeukaryotes using 91 metagenomes from surface down to bathypelagic layers in different oceans, unveiling a clear separation of taxonomic groups between size fractions and depth layers.

Overall, this study shows metagenomics as an excellent resource for taxonomic exploration of marine microbial eukaryotes.

Summary of the relevance of main eukaryotic taxonomic groups within two size fractions of marine plankton (picoeukaryotes [0.2-3 µm] and nanoeukaryotes [3-20µm]) and in two different layers of the global ocean (photic [0-200 m] and aphotic [200-4000m]) as seen by metagenomics. The median of the relative abundance was calculated for each taxonomic group with samples from the 4 categories (pico-photic, pico-aphotic, nano-photic, nano-aphotic) and dots represent these median values transformed to a 0-100 scale. Dots are then colored based on the category where the taxonomic group is most relevant.

This summary was written by the study’s first author, Aleix Obiol.

Full article:
Obiol, A., Giner, C. R., Sánchez, P., Duarte, C. M., Acinas, S. G., & Massana, R. (2020). A metagenomic assessment of microbial eukaryotic diversity in the global ocean. Molecular Ecology Resources. https://doi.org/10.1111/1755-0998.13147

Summary from the authors: Latent Dirichlet Allocation reveals spatial and taxonomic structure in a DNA-based census of soil biodiversity from a tropical forest

Biodiversity inventories can now be built by collecting and sequencing DNA from the environment, which is not only easier, faster and cheaper than direct observation, but also much more comprehensive and systematic. This gives in particular unprecedented access to little-known microbial diversity. Tapping these data to answer community ecology questions, however, can prove a daunting task, as classical statistical approaches often fall short of the size and complexity of molecular datasets. To uncover the spatial structure of soil biodiversity over 12 ha of primary tropical forest in French Guiana, we borrowed a probabilistic model from text analysis. After demonstrating the performance of the method on simulated data, we used it to capture the co-occurrence and covariance patterns of more than 25,000 taxa of bacteria, protists, fungi and metazoans across 1,131 soil samples, collected every 10 m – a dataset that led to a previous publication in Mol. Ecol. (Zinger et al. 2019). We find that, even though the forest plot is at first sight rather uniform, bacteria, protists and fungi are all clearly structured into three assemblages matching the environmental heterogeneity of the plot, whereas metazoans are unstructured at that scale. We then work though the practical problems ecologists may encounter using this approach, such as whether to use presence-absence or read-count data, how to choose the number of assemblages and how to assess the robustness of the results. Finally, we discuss the potential use of related methods in community ecology and biogeography, and argue that probabilistic models are a way forward for analyzing the ever-expanding amount of data generated by the field.

Left: Primary tropical forest understory on the plot where the data were collected, Nouragues ecological research station, French Guiana. Right: Spatial distribution of assemblages of co-occurring soil taxa (OTUs), obtained by Latent Dirichlet Allocation from OTU presence-absence information only, over a 12-ha plot of plateau forest sampled every 10 m (top); and two main axes of environmental variation over the same forest plot, derived from Airborne Laser Scanning (bottom). Bacteria, protists and fungi exhibit a spatial pattern matching the environmental heterogeneity of the plot: the blue, green and red assemblages match the terra firme, hydromorphic and exposed rock parts of the plot, respectively. In contrast, metazoans such as annelids can be shown to be spatially unstructured at that scale. Sampled locations are indicated by dark dots, and values have been interpolated between samples using kriging.

Full article:
Sommeria-Klein G, Zinger L, Coissac E, et al. (2020). Latent Dirichlet Allocation reveals spatial and taxonomic structure in a DNA-based census of soil biodiversity from a tropical forest. Molecular Ecology Resour. 20:371–386. https://doi.org/10.1111/1755-0998.13109

References:
Zinger, L., Taberlet, P., et al. (2019). Body size determines soil community assembly
in a tropical forest. Molecular Ecology, 28(3), 528–543. https://doi.org/10.1111/mec.14919

Summary from the authors: inbreeding and management in captive populations

Pacific salmon hatcheries aim to supplement declining wild populations and support commercial and recreational fisheries. However, there are also risks associated with hatcheries because the captive and wild environments are inherently different. It is important to understand these risks in order to maximize the success of hatcheries. Inbreeding, which occurs when related individuals interbreed, is one risk that may inadvertently be higher in hatcheries due to space limitations and other factors. Inbred fish may have reduced fitness and survival compared to non-inbred fish. We quantified inbreeding and its effect on key fitness traits across four generations in two hatchery populations of adult Chinook salmon that were derived from the same source. We utilized recent advancements in DNA sequencing technology, which provide much more precise estimates of inbreeding and its potential effects on fitness. Our results indicate that inbreeding may not be severe in salmon hatcheries, even small ones, provided that appropriate management practices are followed. However, we documented an influence of inbreeding on the phenology of adult spawners, which could have biological implications for individual fitness and population productivity. Our findings provide a better understanding of changes that may occur in hatchery salmon and will further inform research on “best” hatchery practices to minimize potential risks. 

Article: Waters CD, Hard JJ, Fast DE, Knudsen CM, Bosch WJ, Naish KA. 2020. Genomic and phenotypic effects of inbreeding across two different hatchery management regimes in Chinook salmon. Molecular Ecology https://doi.org/10.1111/mec.15356.

Summary from the authors: Individualized mating system estimation using genomic data

Mimulus guttatus

Hermaphroditic species of plants and animal can produce a mixture of outcrossed and self-fertilized offspring. Estimating the relative frequency of these two outcomes, i.e. the outcrossing rate, has been a major focus in the evolutionary study of reproductive strategies. Outcrossing rate is also a key parameter for plant breeding and for conservation efforts. This paper generalizes a Bayesian method to estimate outcrossing rate (BORICE) using genomic data. Application of the program to an experimental study of Mimulus guttatus illustrates estimation (10% of progeny were selfed), and also how inference of mating system parameters can set up “downstream” evolutionary studies. In the Mimulus study, these downstream analyses included pollination biology (the genetic composition of pollen changed over the season) and local adaptation (inversion polymorphisms exhibit unique patterns of micro spatial structure within the population).

-Professor John K Kelly, University of Kansas

Full article: Colicchio, J., Monnahan, P. J., Wessinger, C. A., Brown, K., Kern, J. R., & Kelly, J. K. (2020). Individualized mating system estimation using genomic data. Molecular ecology resources. https://doi.org/10.1111/1755-0998.13094

Summary from the authors: telomere length predicts remaining lifespan

Close-up of an adult common tern with its prey. Photo credit: Andrea Parisi

Telomeres are DNA structures located at the end of chromosomes. They protect the chromosome, but shorten at each cell division. When telomeres get too short, the normal functioning of cells can be impaired. An individual’s telomere length may therefore predict its future lifespan, and understanding individual telomere dynamics could help to understand ageing in general.

Telomere shortening can be accelerated due to stress, thereby acting as a biomarker of an individual’s health status. However, some studies suggest that individual differences in telomere length are already determined at birth, and largely consistent over life.

We investigated individual telomere dynamics in a long-lived seabird, the common tern. The telomere lengths of 387 individuals, aged from 2 to 24 years, were repeatedly sampled across 10 years. We found that an individual’s telomeres shortened as they got older. Telomere shortening was also slightly increased if individuals had produced more chicks in the previous year. However, the correlation between repeated measures of an individual’s telomere length was very high, even with 6 years between measures. Nevertheless, an individual’s telomere length positively predicted its remaining lifespan, leaving the question of whether lifespan is already partly determined at the start of life.

Full article: Bichet C, Bouwhuis S, Bauch C, Verhulst S, Becker PH, Vedder O. 2019. Telomere length is repeatable, shortens with age and reproductive success, and predicts remaining lifespan in a long-lived seabird. Molecular ecology. https://doi.org/10.1111/mec.15331